Effects of brown tide (Aureococcus anophagefferens) on hard clam Mercenaria mercenaria larvae and implications for benthic recruitment

Abstract

Brown tides of Aureococcus anophagefferens occur in shallow mid-Atlantic bays in the USA and attain peak summer densities of ~1000 to 2800 cells µl -1. Blooms coincide with the period of spawning and planktotrophic larval development of the hard clam Mercenaria mercenaria, a commercially important bivalve in the region. This laboratory study investigates the effects of A. anophagefferens (toxic isolate from Provasoli-Guillard Center for Culture of Marine Phytoplankton [CCMP 1708]) on hard clams throughout their larval development as a function of increasing (1) supplement and (2) contributor to total phytoplankton cell volume in the diet. Brown tide consistently inhibited veliger growth rates in a dose-dependent manner, leading to arrested development in the D-stage; yet mortalities varied greatly among larval batches and were attributed to secondary effects of nutritional stress. Growth of larvae exposed for 2 wk to brown tide at 800 cells µl -1 was 89 to 90% less than controls fed Isochrysis galbana (clone T-iso) in both the presence and absence of alternate food. No recovery was observed when larvae were returned to the control diet. However, larvae showed variable intrapopulation susceptibility to brown tide when exposed to a mixed suspension of A. anophagefferens and I. galbana (400 and 50 cells µl -1 , respectively). Exposure to low levels of brown tide (50 cells µl -1 ) resulted in relatively small but significant growth reduction. Larvae had reduced larval clearance rates (ingestion) when exposed to unialgal brown tide, as confirmed by analysis of gut autofluorescence and negative feeding selectivity for A. anophagefferens in a mixed suspension. Therefore, primarily through their inhibitory effects on growth, brown tides at ≥200 cells µl -1 are expected to cause metamorphic failure of hard clam larval populations. These will lead to extended larval life in the plankton and increased vulnerability to secondary mortality factors. In turn, hard clam larvae are expected to make a negligible contribution to microzooplankton grazing on brown tide. KEY WORDS: Brown tide · Aureococcus anophagefferens · Clam larvae · Mercenaria mercenaria Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 331: [147][148][149][150][151][152][153][154][155][156][157][158][159] 2007 Brown tides have caused considerable economic losses by adversely affecting wild and cultured populations of bivalves, including the hard clam Mercenaria mercenaria, which supports valuable commercial and recreational fisheries and aquaculture in Atlantic North America. Brown tides have caused feeding inhibition of adult suspension-feeding bivalves (e.g. M. mercenaria and Mytilus edulis), mass mortalities of adult mussels M. edulis, growth inhibition and recruitment failure of bay scallops Argopecten irradians (reviewed by Bricelj & Lonsdale 1997) and severe (67%) mortalities of 1 mm hard clams (Greenfield et al. 2002). The inability of the hard clam fishery in Great South Bay to recover from over...

Effects of CO2 and the harmful alga Aureococcus anophagefferens on growth and survival of oyster and scallop larvae

“…HAB-forming dinoflagellates have been shown to cause mortality in multiple species of bi valve larvae, including eastern oysters Crassostrea virginica (Springer et al 2002, Leverone et al 2006, Stoecker et al 2008, Tang & Gobler 2009, northern quahogs Mercenaria mercenaria (Leverone et al 2006, Tang & Gobler 2009, bay scallops Argopecten irradians irradians and A. i. concentricus (Springer et al 2002, Yan et al 2003, Leverone et al 2006, Tang & Gobler 2009, and Japanese scallops Chlamys farreri (Yan et al 2001). In addition, the brown tide-forming pelagophyte Aureococcus ano pha gefferens has been shown to reduce survival, growth, and lipid content of northern quahog larvae (Padilla et al 2006, Bricelj & MacQuarrie 2007 and can slow the growth of larval bay scallops (Gallager et al 1989).Elevated concentrations of carbon dioxide (CO 2 ) are also a significant threat to coastal bivalve populations. CO 2 levels have risen by 40% since the industrial revolution (Caldeira & Wickett 2003), and the rate of increase has tripled since the mid-20th century (Fussel 2009, Friedlingstein et al 2010.…”

Phytoplankton Index of Biotic Integrity and Reference Communities for Barnegat Bay–Little Egg Harbor, New Jersey: A Pilot Study

“…On the other hand, in adult suspensionfeeding bivalves, Aureococcus can inhibit the activity of lateral cilia in the gill (Gainey and Shumway 1991), thereby reducing their growth (Bricelj 1999). In BB-LEH, the reduced growth in juvenile clams has been reported in association with high density of brown tide (Bricelj and MacQuarrie 2007). Studies show that 35% of the state's SAV (submerged aquatic vegetation) habitat in BB-LEH is at significant risk of negative impacts due to brown tide blooms (Gastrich et al 2004).…”

Impact of the toxic dinoflagellateAlexandrium catenellaon Pacific oyster reproductive output: application of flow cytometry assays on spermatozoa

“…More recently, Heterocapsa circularisquama has been shown to reduce activity rate and swimming velocity of spermatozoa of Japanese pearl oyster, Pinctada fucata martensi (Basti et al 2013). Several studies have also reported recruitment failure of various bivalve species following HABs (Granmo et al 1988;Summerson and Peterson 1990;Leverone et al 2006;Bricelj and MacQuarrie 2007;Tang and Gobler 2009), suggesting a potential impact on gamete quality. Indeed, reproductive output and success is at least partially dependent on gamete quality, as it can influence fertilization, embryogenesis and larval development in free-spawning shellfish (Lewis and Ford 2012).…”

“…Assessment of sperm cellular characteristics in cultivated and "exploited" areas could serve as a complementary tool for predicting reduced or unsuccessful recruitment sometimes observed in the field (Granmo et al 1988;Summerson and Peterson 1990;Leverone et al 2006;Bricelj and MacQuarrie 2007;Tang and Gobler 2009).…”